Interpretive Summary: Over twenty percent of the U.S. land area and approximately forty percent of the world’s arable lands are acidic (pH < 5). On these acid soils, aluminum (Al) toxicity is the primary factor limiting agricultural productivity, as toxic Al results in damaged and stunted plant root systems, ultimately resulting in a reduction of crop yields. Given that a large proportion of the acid soils are found in the tropics/subtropics regions where many developing countries are located, Al toxicity limits agricultural productivity in the very areas where food security is most tenuous. Because of the importance of this problem to agriculture worldwide, there is considerable interest and research effort by researchers at universities, government agencies, and international agriculture organizations in identifying genes that provide tolerance to Al toxicity in order to improve crop Al tolerance via molecular breeding and biotechnology. Rice is the most Al tolerant cereal and is a good model for identifying novel Al tolerance mechanisms and genes. In this study, we verified that one of the mechanisms rice uses for Al tolerance involves the uptake of Al from the root cell wall into the cell. Most of the toxic Al in the rice root resides in the cell wall and this mechanism transfers a significant portion of this cell wall Al into the cell, where it is sequestered and detoxified in the cell vacuole. This helps protect the root cell wall from toxic effects of Al. We found that natural variation in the DNA sequence of the Al uptake transporter mediating this Al uptake underlies a significant portion of the variation in rice Al tolerance. That is, tolerant versions of this transporter are much more effective at absorbing Al than sensitive versions. We also found when we transformed the model plant species Arabidopsis with this rice transporter, the transgenic Arabidopsis were much more Al tolerant. These findings suggests that the gene encoding this Al transporter may be a useful tool for enhancing Al tolerance in a wide range of plant species, including other important cereal crop species like corn, wheat and sorghum.

Technical Abstract:
Aluminum (Al) toxicity is a major constraint for crop production on acid soils which comprise approximately 40% of arable land in the tropics and subtropics. Rice is the most Al tolerant cereal crop, and offers a good model for identifying Al tolerance genes and mechanisms. Here we investigated natural variation in the rice NRAT1 gene encoding a root plasma membrane Al uptake transporter previously hypothesized to underlie a unique Al tolerance mechanism. DNA sequence variation in the NRAT1 coding and regulatory regions was associated with changes in NRAT1 expression and NRAT1 Al transport properties. These sequence changes resulted in significant differences in Al tolerance that were found to be associated with changes in the Al content of root cell wall and cell sap in 24 representative rice lines from a rice association panel. Expression of the tolerant OsNRAT1 allele in yeast resulted in higher Al uptake than did the sensitive allele, and conferred greater Al tolerance when expressed in transgenic Arabidopsis. These findings indicate that NRAT1 plays an important role in rice Al tolerance by reducing the level of toxic Al in the root cell wall and transporting Al into the root cell, where it is ultimately sequestered in the vacuole. Given its ability to enhance Al tolerance in rice and Arabidopsis, this work suggests that the NRAT1 gene or its orthologs may be useful tools for enhancing Al tolerance in a wide range of plant species.